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Caveolin-1 selectively regulates microRNA sorting into microvesicles after noxious stimuli

Lee, Heedoo, Li, Chunhua, Zhang, Yang, Zhang, Duo, Otterbein, Leo E., Jin, Yang·2019·Journal of Experimental Medicine
DOI 10.1084/jem.20182313PMC PMC6719430
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Abstract

Emerging evidence suggests that extracellular vesicle (EV)–containing miRNAs mediate intercellular communications in response to noxious stimuli. It remains unclear how a cell selectively sorts the cellular miRNAs into EVs. We report that caveolin-1 (cav-1) is essential for sorting of selected miRNAs into microvesicles (MVs), a main type of EVs generated by outward budding of the plasma membrane. We found that cav-1 tyrosine 14 (Y14)–phosphorylation leads to interactions between cav-1 and hnRNPA2B1, an RNA-binding protein. The cav-1/hnRNPA2B1 complex subsequently traffics together into MVs. Oxidative stress induces O-GlcNAcylation of hnRNPA2B1, resulting in a robustly altered hnRNPA2B1-bound miRNA repertoire. Notably, cav-1 pY14 also promotes hnRNPA2B1 O-GlcNAcylation. Functionally, macrophages serve as the principal recipient of epithelial MVs in the lung. MV-containing cav-1/hnRNPA2B1 complex-bound miR-17/93 activate tissue macrophages. Collectively, cav-1 is the first identified membranous protein that directly guides RNA-binding protein into EVs. Our work delineates a novel mechanism by which oxidative stress compels epithelial cells to package and secrete specific miRNAs and elicits an innate immune response.

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Metadata

Authors
Lee, H., Li, C., Zhang, Y., Zhang, D., Otterbein, L. E., & Jin, Y.
Affiliations
  • Division of Pulmonary and Critical Care Medicine, Department of Medicine, Boston University Medical Campus, Boston, MA 1
  • Department of Computational Medicine and Bioinformatics Department of Biological Chemistry, The University of Michigan, Ann Arbor, MI 2
  • Department of Surgery, Harvard Medical School, Beth Israel Deaconess Medical Center, Boston, MA 3
ORCID
Venue
Journal of Experimental Medicine
Publisher
Rockefeller University Press
Published
2019-06-24
Volume
216
Issue
9
Pages
2202-2220
ISSN
  • 0022-1007
  • 1540-9538
DOI
10.1084/jem.20182313
PMC
PMC6719430
Cited by
219
References
4
Language
en
Licence
Funders
  • National Institutes of Health (R21 AI121644, R33 AI121644R01, R01 GM127596-01, R01 GM111313)
  • U.S. Department of Defense (W81XWH-16-0464)

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